Sage Journals: Discover world-class research

Abstract

Calcicoles are never new to the evolutionary life forms in the ecological world. The ramifications of environmental extremes always facilitate the emergence of the functional and structural integrity of plants and calcicoles, which have been exuding through this. The word “calcicole” finds its roots in the writings of Nathaniel Colgan, “The Orchids of Country Dublin,” published in August 1895 in “The Irish Naturalist.” Calcicoles are likely to flourish under calcium-rich soil having a pH of more than five, which otherwise hinders the growth of plant species, causing detrimental effects on their physiology. They are often regarded as lime lovers or acidofuges and are classified based on Ca²⁺ stress resistance, soluble and insoluble Ca²⁺ and Mg²⁺, pH conditions of soil, occurrence, and habitat. There are various variables used to evaluate the calcicoles described in this review, such as the Index of calcifugy, Ellenberg’s indicator values, and Landolt indicator values to predict the influence of environmental factors in determining flora along with changes in vegetation in a particular area considering the ecophysiological or morphological features. Calcicoles have specific in-built mechanisms to cope with stress conditions by producing phytosiderophores (PS) and by involving ecto and ericoid mycorrhizal associations for the absorption of iron and phosphorus, and high control over cytosolic Ca²⁺ concentrations. Calcicoles are markedly distributed in various plant families like Asteraceae, Brassicaceae, Amaranthaceae, Caryophyllaceae, Ericaceae, Primulaceae, Fabaceae, Gentianaceae, Rubiaceae, Plantaginaceae, Poaceae, Saxifragaceae, etc. The current review focuses on the ecological perspectives, special adaptive features, and phytopharmacological aspects of calcicoles.

Keywords

Calcium calcicoles calcifuge calcareous soil

Introduction

Franz Unger, an Austrian plant physiologist, accentuated geological formation for plant distribution and proposed substrates in his chemical theory of soil, stating that inorganic compounds present in the soil might be a reason for plant distribution of specific substrates.¹ In contrast to the chemical theory of soil, Thurmann proposed a relationship focusing on the physical attributes of soil rather than the chemical composition.² Later, scholars contemplated edaphic factors while explaining this relationship, which encompasses chemical and physical parameters.³ The presence or absence of specific types of inorganic compounds in the soil is responsible for different floral patterns in distinct habitats.⁴ The inorganic compound calcium is a fundamentally required nutrient for optimum plant growth and development.⁵ This biomineral⁶ has a significant role in maintaining the functional and structural integrity of cell membranes⁷ and also serves as an intracellular second messenger in plants.⁸ Calcium plays a decisive role in adapting plants in different environmental extremes⁹ and abiotic stresses.¹⁰ Calcium deficiency in plants decrease the development of terminal shoot buds and apical root tips, inhibiting plant growth.¹¹ The calcium excess is also detrimental to plant health.¹² Plants can be classified as calcicoles and calcifuges based on their calcium requirements.¹³ Only calcicoles have developed unique adaptive mechanisms to cope with excessive calcium in the soil.¹⁴

Calcicoles

The word calcicole finds its roots in the writings of Nathaniel Colgan, “The Orchids of Country Dublin,” published in August 1895 in “The Irish Naturalist.” He mentioned Orchis pyramidalis as a calcicole plant abundantly distributed in Dublin and he adopted this word from M. Coutejean’s “Geographic Botanique” Paris, 1881.¹⁵ These are calcium-loving plants capable of thriving in elevated calcium levels¹⁶ or soils with high pH and are often regarded as chalk-loving or acidifuge plants.¹⁷ Calcicoles like to flourish under calcareous soil¹⁸ majorly well-drained,¹⁹ whereas calcifuge encompasses lime-avoiding plants.²⁰ Barkman in 1958 suggested replacing the term for calcium-loving plants “calciphilous” with the term “calciphyte” due to the distinct ecophysiological behavior of plants.²¹ However, the term “calcicole” continued to flourish and was also investigated by ecologists as a separate identity or class because of its diverse adaptive characteristics.²² Plants species belonging to the same genus are found to flourish under different soil conditions, some examples of these vicarious distributions include Achillea atrata, Carex firma, Doronicum grandiflorum, Gentiana clusii, Hutchinsia alpina, Pedicularis rostratocapitata, Primula auricular, Saxifraga moschata predominantly inhabits in calcareous soils whereas Achillea moschata, Carex curvula, Doronicum clusii, Gentiana kochiana, Hutchinsia sulphurea, Pedicularis kerneri, Primula hirsuta, Saxifraga exarata inhabited as calcifuge.²³

Methodology

The current study encompasses a systematic review of calcicoles, concerning their origin, mechanisms, distribution, comparison with calcifuges, and phytopharmacological status. Various databases viz. PubMed, Francis & Taylor, Sci-Hub, SciFinder, Google Scholar, SciELO, and Springer have been thoroughly explored to frame this review article.

Calcicole v/s Calcifuge

With evolution, plants have developed different mechanisms to counter varying conditions of soil, like pH and calcium concentration. Ecologists designated them as calcicoles and calcifuges based on their endurance in distinct soil conditions.²⁴ The differences between various aspects of calcicole and calcifuge are summarized as follows:

Calcicoles (acidofuges) are lime lovers and typically dwell on chalk, whereas calcifuge (acidophiles) are lime avoiders predominantly found on lowland heath.^{25, 26}

Calcicoles flourish on alkaline soil with a pH ranging between 5 and 7 (moderate), and greater than 7 (extreme) whereas calcifuges prefer acidic soil with less than pH 5.^27–29

Calcicoles usually do not resist aluminum in the root environment compared to calcifuge, which resists the higher soluble Al³⁺ in root concentration.³⁰

Most calcicoles are insensitive to Fe concentration in contrast to calcifuge, which can tolerate high Fe soil concentrations.^{27, 31}

Calcicoles have higher control over cytosolic Ca2+ concentrations than calcifuges.³²

Calcicoles better utilize NO₃-N (nitrate-nitrogen) when compared against calcifuge which showed optimum growth with NH₄-N (ammonium nitrogen).^{33, 34}

Mycorrhizal fungi associations are usually higher in calcicoles than calcifuges.³⁵

Calcicoles have unique mechanisms to solubilize iron and phosphates whereas this property is absent in calcifuges.^{27, 36}

Root exudates of calcicoles secrete more citric and oxalic acid when compared with calcifuges.³⁰

Calcicoles are more efficient in producing phytosiderophores (PS) than calcifuges.³⁷

A brief comparison of calcicole and calcifuge is summarized in Table 1.

Table 1.

Comparison Between Calcicole and Calcifuge.

Sl. No.	Basis for Comparison	Calcicole	Calcifuge	Reference
1.	The root word (Latin)	To dwell on chalk-lime lovers	To flee from chalk-lime avoiders	²⁵
2.	Synonyms	Acidofuges, calciphilous	Acidophiles, calciophobes	^{38, 39}
3.	Distribution among plant communities	Chalk grassland, karst region	Lowland heath	²⁶
4.	Substrate preference (Soil)	Alkaline	Acidic	²⁹
5.	Examples	Achillea atrata Carex firma Doronicum grandiflorum	Achillea moschata Carex curvula Doronicum clusii	²³
6.	pH	Extreme calciocoles pH>7, Moderate calciocoles pH 5-7	pH <5	²⁸
7.	Al³⁺ concentration	Do not resist aluminum in the root environment	Resist higher levels of soluble Al³⁺ in root concentration	³⁰
8.	Oxalic and citric acid excretion	Excrete more oxalic acid and citric acid	Excrete has less amount of oxalic and citric acid than calcicoles	^{30, 40}
9.	Iron deficiency	Insensitive	Can tolerate high soil concentrations	^{27, 31}
10.	Phosphorous solubilization	The solubilization of inorganic phosphate and iron by carboxylate exudation in calcicoles inevitably also enhances the concentration of calcium	Calcifuge species solubilize phosphorous	²⁷
11.	Control over cytosolic Ca²⁺ concentrations	High	Poor	³²
12.	Solubilize iron and phosphates	Unique mechanisms to solubilize iron and phosphates	Inability to solubilize iron and phosphates when grown in calcareous soil	³⁶
13.	Nitrogen source	Calcicoles better utilize NO₃-N (nitrate nitrogen)	Growth is optimal with NH₄-N (ammonium nitrogen)	^{33, 34}
14	Mycorrhizal fungi associations	High	Low	³⁵
15.	Phytosiderophores	Efficient in producing phytosiderophores	Less efficient than calcicoles in producing phytosiderophores	³⁷

Classification of Calcicoles

As all calcium-rich soils are not alkaline and calcareous, so calcicoles are not restricted to thriving in calcareous soils.^{41, 42} investigated several calcicolous habitats and subdivided calcicolous flora based on the environmental occurrence of species into pseudo-calcicolous (frequently found on calcareous soil) and oxyphobic (species intolerant of high soil acidities).¹⁹ investigated different plant communities inhabiting limestones and granite soils and classified calcicoles based on the ratio of soluble to insoluble Ca²⁺, and Mg²⁺ in the leaves into obligate and facultative calcicoles.⁴³ Etherington, 1982 studied the basis of pH conditions of soil into extreme calcicoles (pH >7) and moderate calcicoles (pH 5-7). They are also distinguished plants based on Ca²⁺ stress resistance in them, that is, calciophobes (calcium-avoiding plants) and calciophiles (calcium-loving plants).²⁸ Species that occur only in calcareous soils/habitats are strict calcicoles, whereas those that can tolerate siliceous soil but largely prefer calcareous soil are non-strict calcicoles.⁴⁴ Calcicoles inhabited in warm and dry conditions of the Mediterranean are termed thermal calcicoles.^{45, 46} Classification of calcicoles is summarized in Figure 1.

Figure 1.

Classification of Calcicoles.

Distribution of Calcicoles

Calcicole distribution is marked by the high calcium solubility in calcareous rocks as they usually thrive in soil rich in calcium carbonate.⁴⁷ Calcium in the form of calcium phosphate has commonly been observed in several species belonging to Brassicales, Boraginales, and Malpighiales order.⁶ Calcicoles are also well distributed among moss taxa including Tortula mucronifolia, Schistidium apocarpum, Grimmia anodon, Gymnostomum, Bryum argenteum, etc.⁴⁷ Karst ecosystem offers a distinct environment that facilitates the growth of calcicole plants with unique characteristics.⁴⁸ Several chalkland grassland communities of grasses like Festuca ovina, Avenula pratensis are calcicoles.⁴⁹ Several calcicoles viz. cabbage, broccoli, and kale of Brassicaceae have established themselves as food utilized for human consumption.⁵⁰Cucumis sativus, Leiocolea rutheana, and Koeleria gracilis are examples of obligate calcicoles.^51–53 The distribution of calcicoles is represented in Table 2, as indicated below in this review.

Table 2.

Distribution of Calcicoles.

Order	Family	Genus	Species	Common Name	References
Asterales	Asteraceae	Achillea	A. atrata	Black yarrow	¹⁹
		Doronicum	D. grandiflorum	Leopard’s-bane	²³
		Lactuca	L. sativa	Lettuce	²³
		Artemisia	A. rupestris	Rock wormwood	⁵⁴
		Leontodon	L. hispidus	Bristly hawkbit	⁵
		Centaurea	C. scabiosa	Greater knapweed	⁵
Apiales	Apiaceae	Pimpinella	P. saxifrage	Burnet saxifrage	⁵⁵
Brassicales	Brassicaceae	Hutchinsia	Hutchinsia alpina	Chamois cress	²³
Brassicales	Brassicaceae	Arabis	A. hirsuta	Hairy rock-cress	⁵⁶
Caryophyllales	Amaranthaceae	Beta	B. vulgaris	Beet	²³
	Caryophyllaceae	Gypsophila	G. fastigiata	Baby’s-breath	⁵⁴
	Caryophyllaceae	Silene	S. uniflora	Sea campion	³⁶
Celastrales	Celastraceae	Parnassia	P. palustris	Marsh grass of parnassus	⁵⁶
Dipsacales	Caprifoliaceae	Scabiosa	S. columbaria	Small scabious	²³
Ericales	Ericaceae	Rhododendron	R. hirsutum	Hairy alpenrose	⁵⁷
	Primulaceae	Primula	P. auricula	Bear’s ear	²³
	Primulaceae	Soldanella	S. alpina	Blue moonwort	²³
Fabales	Fabaceae	Medicago	M. sativa	Alfa alfa	⁵⁸
		Oxytropis	O. campestris	Field locoweed	⁵⁴
		Anthyllis	A. vulneraria	Common kidney vetch	⁵⁶
	Fagaceae	Cyclobalanopsis	C. glauca	Japanese blue oak	⁵⁹
Gentianales	Gentianaceae	Gentiana	G. clusii	Flower of the sweet-lady	²³
Gentianales	Rubiaceae	Asperula	A. cynanchica	Squinancy wort	⁶⁰
Lamiales	Orobanchaceae	Pedicularis	Pedicularis rostratocapitata	Long-nosed lousewort	²³
Lamiales	Plantaginaceae	Veronica	V. spicata	Spiked speedwell	⁵⁴
Lecanorales	Cladoniaceae	Cladonia	C. rangiformis	Reindeer cup lichen	⁶¹
Malpighiales	Violaceae	Viola	V. hirta	Sweet violet	⁵⁴
Malvales	Malvaceae	Cola	C. porphyrantha	—	⁶²
Poales	Cyperaceae	Carex	C. firma	Sedge	²³
	Poaceae	Sesleria	S. caerulea	Blue moor grass	²³
		Hordeum	H. vulgare	Barley	²³
		Triticum	T. aestivum	Common wheat	⁶³
		Agrostis	A. stolonifera	Creeping bentgrass	⁶⁴
		Festuca	F. pratensis	Meadow fescue	²³
		Melica	M. ciliate	Hairy melic	³⁶
		Phleum	P. phleoides	Boehmer’s cat’s-tail	³⁶
Polypodiales	Pteridaceae	Adiantum capillus-veneris	A. dissectum	Southern maidenhair fern	⁶⁵
	Pteridaceae	Adiantum	A. malesianum	–	⁶⁵
	Aspleniaceae	Asplenium	A. scolopendrium	Hart’s tongue fern	⁶⁶
	Aspleniaceae	Asplenium	A. trichomanes subsp. quadrivalens	Maidenhair spleenwort	⁶⁶
	Polypodiineae	Polystichum	P. aculeatum	Hard shield-fern	⁶⁶
	Dryopteridaceae	Polystichum	P. setiferum	Soft shield-fern	⁶⁶
	Aspleniaceae	Asplenium	A. viride	Green spleenwort	⁶⁷
Proteales	Proteaceae	Grevillea	G. thelemanniana	Spider-net grevillea	⁴¹
Ranunculales	Ranunculaceae	Pulsatilla	P. alpina	Pasque flower	⁶⁸
Ranunculales	Ranunculaceae	Ranunculus	R. alpestris	Alpine buttercup	⁶⁹
Rosales	Rosaceae	Potentilla	P. verna	Spring cinquefoil	⁷⁰
	Rosaceae	Sanguisorba	S. minor	Salad burnet	³⁶
	Urticaceae	Parietaria	P. diffusa	Pellitory of the wall	⁷¹
	Ulmaceae	Ulmus	U. minor	Field elm	⁷²
Salicaceae	Malpighiales	Salix	S. reticulata	Snow willow	⁷³
Saxifragales	Saxifragaceae	Saxifraga	Saxifraga moschata	Mossy saxifrage	²³
Saxifragales	Saxifragaceae	Saxifraga	S. aizoides	Yellow mountain saxifrage	⁷⁴

Adaptive Mechanism of Calcicoles

Calcicoles have a unique ability to tolerate and avoid high calcium concentrations in plants. Some of the members of Brassicaceae are calciotrophic, which can accumulate a large amount of soluble calcium in vacuoles, thereby providing a decisive role in osmoregulation, particularly in dry limestone areas.⁷⁵ In a few calcicoles, the calcium uptake is more restricted compared to calcifuge species because of less affinity of root plasma membranes for calcium ions.³⁵ Calcicoles have built adaptive mechanisms to counteract high concentrations of calcium and bicarbonates and flourish under low Fe, Zn availability.⁷⁶ Multiple ecto and ericoid mycorrhizal associations were found among calcicoles. Carex sempervirens, Polygonum viviparum, and Festuca pumila are associated with endomycorrhizal infection.⁷⁷ Mycorrhizal fungus aids in promoting tolerance in plants inhabited in calcareous soil conditions.⁷⁸ The fungus can release siderophores, produce organic acids, and enhance Fe acquisition which aids in dissolving calcium phosphates thereby promulgating adaptive behaviors in plants by removing recessive Ca uptake via precipitating calcium oxalate around fungal hyphae.^{35, 79–81} These PS can chelate Fe or Zn, thereby increasing their uptake by plants⁸² and having a prominent role in the acquisition of Fe and are reported to be produced in various Graminaceous species.⁸³ PS are organic chelating compounds excreted by the roots of plants like rice, barley, oats, wheat, etc., belonging to the grass family.⁸⁴ PS are also secreted by several calcioles thereby promulgating adaptive behavior.⁸⁵ Hordelymus europaeus, a calcicole grass can produce PS when grown under Fe, Cu deficiencies.⁸⁶ demonstrated the role of PS in Fe-limiting conditions in different calcicole species belonging to Poaceae.⁸⁷ PS production significantly increased during Fe deficiency and facilitated their survival in calcareous habitats. successfully demonstrated calcium accumulation in calcicole strain due to ectomycorrhizal fungus Paxillus involutus.⁸⁸ Calcicoles can store excess amounts of calcium in the form of crystals³⁰; epidermal cells also play a significant role in Ca sequestration.¹⁷ Calcium concentration is predominantly concentrated in the distal tips of leaf trichomes and epidermal cells.⁸⁹ Several studies have reported that the epidermal tissue, particularly the trichome tip cell of calcicoles Centaurea scabiosa and Leontodon hispidus contains a high amount of calcium and serves as a site for its deposition facilitating a protection mechanism in calcicoles.⁷⁶ reported improvements in antioxidant defense, osmotic level, water status, and photosynthesis efficiency in calcicole species Cyclobalanopsis glauca upon exogenous administration of Ca²⁺ when grown under drought stress conditions.⁵⁹ reported calcium distribution in Lavandula pinnata and explained its role in gland development.⁹⁰ reported that IMA peptides (IRONMAN peptides) are involved in regulating Fe uptake by controlling gene expression in calcicoles, which permits them to adapt in calcareous soil conditions.⁹¹ The above-mentioned mechanisms that are involved are also highlighted in Figure 2.

Figure 2.

Adaptive Mechanism in Calcicoles. (1) Accumulation of Soluble Calcium in Vacuoles for Osmoregulation. (2) Calcium Concentration in Distal Tips of Leaf Trichomes and Epidermal Cells. (3) Phytosideophores can Chelate Fe or Zn. (4) Multiple Ecto and Ericoid Mycorrhizal Associations Result in the Accumulation of Calcium Around Fungal Hyphae. (5) IMA Peptides Regulate Iron Uptake. (6) Lower Affinity for Root Plasma Membrane of Calcium.

Indexes and Indicator Values

Ecologists have developed different indexes and indicator values to explain calcifuge/calcicole behaviors of plants, as described in this review.

Index of Calcifugy

A book entitled “An Ecological Atlas of Grassland Plants” authored by J. Philip Grime and Philip S. Lloyd, mentioned autecological comparative studies of common grassland species of (Sheffield) Britain. They critically examined the area’s ecology and presented their work using pH tables, grazing/burning tables, and pH histograms. Later, in 1981, Etherington calculated an Index of calcifugy for different plant species using histograms of species constancy prepared by Grime & Lloyd in 1973. Etherington demonstrated the calcifuge index (IC) as represented below by employing a formula and classifying plants with emphasis on pH, which gave further insights into calcifuge species.⁹²

Calcifuge Index = \frac{Constancy in classes of pH < 5.5}{Constancy in all pH classes} \times 100

Cross & Lambers critically examined calcicole and calcifuge plant strategies, along with their nutrient-acquisition relationship in around 538 plant species using histograms of species constancy in 0.5 pH unit classes prepared by Grime and Lloyd, 1973 and Etherington calcifuge index, 1981 and they further classified plant species based upon the index as represented in Table 3. Plant species having an IC value of 0 were regarded as calcicoles.²⁷

Table 3.

Calcifuge Index (IC) Values of Different Plant Species Predicted by Cross and Lambers, 2021.

Calcifuge Index (IC)	Species
100	Likely calcifuge
75–99	Possibly calcifuge
26–74	Soil indifferent
1–25	Likely not calcifuge
0	Highly likely not calcifuge or calcicole

Ellenberg’s Indicator Values

Heinz Ellenberg, a German ecologist, developed nine-point scales for plant preferences and suggested indicator values, and they have been used to predict the influence of several environmental factors in determining flora along with changes in vegetation in a particular area considering the ecophysiological or morphological features like temperature, light, moisture, continentality, soil reaction, salinity, nutrients.^{93, 94} Ellenberg assigned different numbers from 1 to 5 or (0) 1 to 9 (10) indicating the preferences for increasing the availability of resources. These values established by Ellenberg were particularly in the context of European conditions²² and have also been validated on different flora belonging to diverse geographical conditions viz. Switzerland,⁹⁵ Czech,⁹⁶ Britain,⁹⁷ Itlay,⁹⁸ Sweden,⁹⁹ Faroe Islands¹⁰⁰ etc. EIVs can also be successfully employed for monitoring changes in the environment.¹⁰¹ Ewald employed Ellenberg indicator values of soil reaction (R values) about calcicole species and distinguished calcicoles based on R value. Species with R values 7 and 9 represent moderately acid to moderately basic conditions and indicators of bases and lime, respectively. R value 8, that is, intermediate between 7 and 9, indicating the presence of lime.¹⁰² EIVs have been illustrated in Figure 3, emphasizing the reaction of soil values (pH).¹⁰³

Figure 3.

Ellenberg Indicator Values.

Landolt Indicator Values

Elias Landolt, a Swiss geobotanist, developed reaction indicator values (RL) 95 and uses the term humidity index considering different conditions, viz. moisture, nutrient availability, acidity, etc., mainly for Switzerland. Landolt assigned an integer between 1 and 5 to plant species depending on their ability to combat stress like water, soil acidity, lack of nutrients, shade, etc.¹⁰⁴ Plant species with R_L value 1 (pH 3–4.5) are indicators of excessive acidity and termed strict calcifuges. In contrast, species with R_L value 5 (pH > 6.5) are distributed on calcareous soils and indicators of primary reaction, termed strict calcicoles.^{105, 106} The indicator values developed by Landolt have been successfully tested by several ecologists viz. Nakhutsrishvili et al. developed new indicator values of vascular plants of the Caucasus area by comparing them with Landolt indicator values of alpine plants, and the results showed high overlapping of values (30%–50% congruence).¹⁰⁵

Phytopharmacological Status of Calcicoles

Thorough research on calcicole species is essential for a better understanding of their elevated calcium mechanism and their exploration for pharmacological use. We have reported the phytopharmacological status of various calcicole species here by critically examining the scientific reports from authorized databases in Table 4. This review inculcated anti-inflammatory activity in Beta vulgaris,¹⁰⁷ Leontodon hispidus,¹⁰⁸ Ulmus minor.¹⁰⁹ Antioxidant activity in Anthyllis vulneraria,¹¹⁰ Veronica spicata,¹¹¹ Lactuca sativa,¹¹² Triticum aestivum,¹¹³ Scabiosa columbaria.¹¹⁴ Antimicrobial activity in Cladonia rangiformis,¹¹⁵ A. atrata,¹¹⁶ Artemisia rupestris,¹¹⁷ Polystichum aculeatum,¹¹⁸ Centaurea scabiosa,¹¹⁹ Medicago sativa.¹²⁰ Other pharmacological activities include CNS depressive effects in Pulsatilla alpina,¹²¹ antiurolithiatic activity in Hordeum vulgare etc.¹²²

Anti-inflammatory Activity

Various pharmacological models were used to evaluate anti-inflammatory activity and mechanism of action of calcicole species crude extracts and isolated compounds. The most acceptable results are described here. Betalain-rich beetroot juice 500 ml/day was reported to alleviate inflammatory mediators (TNF-α, INL-6) in osteoarthritic patients when administered to osteoarthritic patients for 10 consecutive days.¹⁰⁶ Sesquiterpene lactone hypocretenolides isolated from Leontodon hispidus exhibited anti-inflammatory action in croton oil-induced mouse ear edema experimental models.¹⁰⁸ Phytoconstituents isolated from Ulmus minor showed anti-inflammatory activity in the macrophage cell line.¹⁰⁹

Antioxidant Activity

Phenolics isolated from the leaf of Woundwort, Anthyllis vulneraria showed antioxidant activity.¹¹⁰ Herb Veronica spicata showed free radical scavenging potential when evaluated in different in vitro models viz. DPPH, β-carotene bleaching assay, reducing power assay.¹¹¹ Bioactive compounds isolated from lettuce, Lactuca sativa have antioxidant potential.¹¹² Phenolics, tocopherols, and carotenoids are attributed to the antioxidant capacity of wheat, Triticum aestivum.¹¹³ Leaf extract of Scabiosa columbaria showed anti-melanogenic and antioxidant effects in human foreskin fibroblast (MRHF) cells, ferric reducing antioxidant power (FRAP) assay, respectively.¹¹⁴

Antimicrobial Activity

Ethanolic and chloroform extract Cladonia rangiformis exhibited moderate antifungal effects when tested against Staphylococcus aureus, Pseudomonas aeruginosa, and Escherichia coli.¹¹⁵ Flavones and sesquiterpene lactones isolated from aerial parts of A. atrata exhibited antimicrobial activity in Bacillus subtilis, Candida albicans, and E. coli.¹¹⁶

Flavonoids (artemetin, chrysoeriol, chrysoplenetin, penduletin, pachypodol) isolated from dichloromethane extract of Artemisia rupestris exhibited showed synergistic effect with ciprofloxacin, norfloxacin and oxacillin when tested against fluoroquinolone-resistant Staphylococcus strain (SA1199B).¹¹⁷ Triterpenoids and polyphenols isolated from methanolic extract of rhizomes of Polystichum aculeatum exhibited anti-bacterial activity against Staphylococcus aureus.¹¹⁸ Extract obtained from flowers of greater knapweed, Centaurea scabiosa showed antimicrobial activity with a minimum inhibitory concentration between 60 and 120 µg/ml.¹¹⁹ Saponin-rich fraction isolated from aerial parts and roots of Medicago sativa exhibited antifungal activity when evaluated against Candida albicans.¹²⁰

Other Pharmacological Activities

The extract obtained from aerial parts of Pulsatilla alpina exhibited CNS depressive effects in pharmacological screening models.¹²¹ Phenolics obtained from ethanolic extract of roots of Beta vulgaris ameliorates nephrotoxicity induced by gentamicin in experimental rat models.¹²³ Extract prepared from seeds of Hordeum vulgare exhibited antiurolithiatic activity when evaluated on Wistar albino rats.¹²² Ethanolic extract of Sanguisorba minor restricts plasmin-mediated tumor cell motility when evaluated in vitro.¹²⁴

Table 4.

Reported Phytopharmacological Potential of Calcicoles.

Plant Name	Family	Part Used	Reported Phytoconstituents	Reported Pharmacological Activity	Reference
Beta vulgaris	Amaranthaceae	Roots	Betalain	Anti-inflammatory	¹⁰⁷
Leontodon hispidus	Asteraceae	Entire plant	Hypocretenolides	Anti-inflammatory	¹⁰⁸
Ulmus minor	Ulmaceae	Root bark	Flavonoids	Osteoarthritis	¹⁰⁹
Anthyllis vulneraria	Fabaceae	Leaf	Phenolics	Antioxidant, anti-bacterial	¹¹⁰
Veronica spicata	Plantaginaceae	Aerial parts	Phenolics	Antioxidant, antimicrobial	¹¹¹
Lactuca sativa	Asteraceae	Leaves	Phenolics, ascorbic acid, carotenoids, lycopene	Antioxidant	¹¹²
Triticum aestivum	Poaceae	Seeds	Carotenoids, tocopherols and tocotrienols	Antioxidant	¹¹³
Scabiosa columbaria	Caprifoliaceae	Leaves	Polyphenols, flavonoids, terpenoids and coumarins	Anti-melanogenesis, antioxidant, anti-tyrosinase activities	¹¹⁴
Cladonia rangiformis	Cladoniaceae	Lichen	Carbohydrates	Antimicrobial activities	¹¹⁵
A. atrata	Asteraceae	Aerial parts	Flavones	Antimicrobial	¹¹⁶
Artemisia rupestris	Asteraceae	Herb	Flavonoids	Anti-bacterial	¹¹⁷
Polystichum aculeatum	Dryopteridaceae	Rhizome	Triterpenoids, polyphenol	Anti-bacterial	¹¹⁸
Centaurea scabiosa	Asteraceae	Flowers	Pyranone, coumaran (2,3-dihydrobenzofuran), 5-hydroxymethylfurfural	Antimicrobial	¹¹⁹
Medicago sativa	Fabaceae	Aerial parts, roots	Saponins	Antifungal activity	¹²⁰
Pulsatilla alpina	Ranunculaceae	Aerial parts	Protoanemonin, anemonin	CNS depressant	¹²¹
Beta vulgaris	Amaranthaceae	Roots	Phenolics	Protective effect on gentamicin-induced nephrotoxicity	¹²³
Sanguisorba minor	Rosaceae	Whole plant	Quercetin-3-glucuronide	Limits plasmin-mediated tumor cell motility	¹²⁴
Salix reticulata	Salicaceae	Aerial parts	Phenolics	Anti-proliferative	¹²⁵
Hordeum vulgare	Poaceae	Seeds	Starch, protein, phenolics, iron	Antiurolithiatic	¹²⁶

Conclusion and Future Perspectives

The main objective of this review is to highlight the importance of calcicoles. Calcicoles can be revived in a more described manner so that further exploration can accentuate the usefulness of calcicoles not only from an ecological point of view but also having nutritional sources and pharmacological significance. It has a significant history of evaluating their distribution along with their phytochemical importance which can be a great source of therapeutic uses too. As calcicoles have developed a unique mechanism to survive under extreme conditions, that is, increased concentration of calcium or basic pH in the rhizosphere, they need to be more scrutinized for their functionality. They have consistently been a topic of discussion because of this inherent mechanism for the accumulation of excess calcium. They are classified as varying in parameters responsible for their growth under different conditions of soil and the micronutrients. Edaphic factors like light, temperature, region, pH, moisture content, soil value, etc. are described by different scholars/ecologists in different ways and suggested various indexes for their implications too like the Calicuge index, Ellenberg, indicator value, and Landolt indicator. Classification of calcicoles based on the ratio of soluble and insoluble calcium, stress resistance, and pH condition, are given in this review to narrate calcicoles more systematically. Phytochemicals reported in calcicoles showed promising biological activities when evaluated on different in-vivo and in vitro experimental models like anti-inflammatory, antioxidant, antimicrobial, antifungal, etc. Importantly, based upon the research findings on the calcium tolerance mechanism in calcicoles will facilitate researchers to work on calcicoles with a distinct perspective. In conclusion, calcicoles have immense potential in the field of ecology and their therapeutic potential has to be explored more scientifically to find new drug candidates from them in drug discovery. In this way this present review is significant and need of hour and the work cited here regarding lime lovers is expected to aid in identifying the ecological and pharmacological potential of calcicoles.

Abbreviations

CNS: Central nervous system; DPPH: 2,2-diphenyl-1-picrylhydrazyl; FRAP: Ferric reducing antioxidant power; IC: index of calcifugy; TNF-α: Tumor necrosis factor-alpha; IL-6: Interleukin 6.

Footnotes

Acknowledgments

The authors sincerely acknowledge Dr. Vivek Sharma, Professor Govt. College of Pharmacy Rohru, and CT University, Ludhiana, Punjab for the support to accomplish this work.

Declaration of Conflicting Interests

The authors declared no potential conflicts of interest with respect to the research, authorship and/or publication of this article.

Ethical Statement

Ethical permission was not applicable for this article, as this is a review article drafted from various research articles and not from patients directly.

Funding

The authors received no financial support for the research, authorship and/or publication of this article.

Informed Consent

Not applicable.

ORCID iDs

Ranjeet Kaur Parmar

Vikrant Arya

References

Ueber den Einfluss UF des Bodens auf die Vertheilung der Gewächse: nachgewiesen in der vegetation des nordöstlichen Tirol’s. Bei Rohrmann und Schweigerd, 1836.

Thurmann

Essai de phytostatique appliqué à la chaîne du Jura et aux contrées voisines: ou Étude de la dispersion des plantes vasculaires envisagée principalement quant à l’influence Des Roches soujacentes. Jent Gassmann, 1849.

Rivas-Goday

Flora serpentinícola española, nota primera (Edafismos endémicos del Reino de Granada). An Real Acad Farm 1969; 35: 297–304.

De Deyn

and Kooistra

The role of soils in habitat creation, maintenance and restoration. Philos Trans R Soc Lond B Biol Sci 2021; 376(1834): 20200170. DOI: 10.1098/rstb.2020.0170, PMID 34365817.

White

and Broadley

MR.

Calcium in plants. Ann Bot 2003; 92(4): 487–511. DOI: 10.1093/aob/mcg164, PMID 12933363.

Weigend

, Mustafa

and Ensikat

HJ.

Calcium phosphate in plant trichomes: the overlooked biomineral. Planta 2018; 247(1): 277–285. DOI: 10.1007/s00425-017-2826-1, PMID 29234879.

Hadi

and Karimi

The role of calcium in plants salt tolerance. J Plant Nutr 2012; 35(13): 2037–2054. DOI: 10.1080/01904167.2012.717158.

Tuteja

and Mahajan

Calcium signaling network in plants: an overview. Plant Signal Behav 2007; 2(2): 79–85. DOI: 10.4161/psb.2.2.4176, PMID 19516972.

Tong

, Li

, Jiang

, . Molecular evolution of calcium signaling and transport in plant adaptation to abiotic stress. Int J Mol Sci 2021; 22(22): 12308. DOI: 10.3390/ijms222212308, PMID 34830190.

10.

Wilkins

, Matthus

, Swarbreck

, . Calcium-mediated abiotic stress signaling in roots. Front Plant Sci 2016; 7: 1296. DOI: 10.3389/fpls.2016.01296, PMID 27621742.

11.

Olle

and Bender

Causes and control of calcium deficiency disorders in vegetables: a review. J Hortic Sci Biotechnol 2009; 84(6): 577–584. DOI: 10.1080/14620316.2009.11512568.

12.

Romero

, Gladon

and Taber

HG.

Effect of excessive calcium applications on growth and postharvest performance of bedding-plant impatiens. J Plant Nutr 2007; 30(10): 1639–1649. DOI: 10.1080/01904160701615517.

13.

Fageria

NK.

The use of nutrients in crop plants . Boca Raton: CRC Press, 2016.

14.

, He

, Tang

, . Adaptation of plants to high-calcium content kart regions: possible involvement of symbiotic microorganisms and underlying mechanisms. Braz J Biol 2020; 80(1): 209–214. DOI: 10.1590/1519-6984.186437, PMID 31116294.

15.

Colgan

The orchids of county Dublin . Dublin: Eason & Son, 1895.

16.

Praeger

RL.

Irish topographical botany . Dublin: Royal Irish Academy, 1901.

17.

Lambers

, Oliveira

, Lambers

, . Mineral nutrition. Plant Physiol Ecol 2019: 301–384. DOI: 10.1007/978-0-387-78341-3

18.

Simpson

JF.

A chalk flora on the lower greensand: its use in interpreting the calcicole habit. J Ecol 1938; 26(1): 218–235. DOI: 10.2307/2256420.

19.

Salisbury

EJ.

The significance of the calcicolous habit. J Ecol 1920; 8(3): 202–215. DOI: 10.2307/2255613.

20.

Janick

Horticultural reviews . Vol. 30. United States: John Wiley & Sons, 2003.

21.

Vos

and Stortelder

Vanishing Tuscan landscapes. Landscape ecology of a submediterranean-montane area (Solano Basin, Tuscany, Italy), 1992.

22.

Korner

Ecology of populations and vegetation. In: Bresinsky

, Körner

, Kadereit

, Neuhaus

and Sonnewald

(eds) Strasburger’s plant sciences . Heidelberg: Heidelberg, 2013, pp. 1167–1215. DOI: 10.1007/978-3-642-15518-5_13.

23.

Larcher

Physiological plant ecology: ecophysiology and stress physiology of functional groups . New York: Springer Science+Business Media, 2003.

24.

Kirkby

and Johnston

AE.

Soil and fertilizer phosphorus in relation to crop nutrition. In: The ecophysiology of plant-phosphorus interactions . New York: Springer, 2008, pp. 177–223. DOI: 10.1007/978-1-4020-8435-5_9.

25.

Lousley

and Atkinson

Wild flowers of chalk & limestone . Vol. 16. London: Collins, 1950.

26.

Jeffrey

DW.

Soil-plant relationships . London: Croom-Helm, 1987.

27.

Cross

and Lambers

Calcicole–calcifuge plant strategies limit restoration potential in a regional semi-arid flora. Ecol Evol 2021;11(11): 6941–6961. DOI: 10.1002/ece3.7544, PMID 34141267.

28.

Huggett

RJ.

Fundamentals of biogeography . New York: Routledge, 2004.

29.

Dixon

Garden practices and their science . New York: Routledge, 2018.

30.

Lambers

, Chapin

and Pons

TL.

Plant physiological ecology . New York: Springer, 2008. DOI: 10.1007/978-0-387-78341-3.

31.

Vélez-Bermúdez

and Schmidt

Plant strategies to mine iron from alkaline substrates. Plant Soil 2023; 483(1–2): 1–25. DOI: 10.1007/s11104-022-05746-1.

32.

Lee

JA.

The calcicole-calcifuge problem revisited. Adv Bot Res 1998; 29: 1–30. DOI: 10.1016/S0065-2296(08)60306-7.

33.

Gigon

and Rorison

IH.

The response of some ecologically distinct plant species to nitrate-and to ammonium-nitrogen. J Ecol 1972; 60(1): 93–102. DOI: 10.2307/2258043.

34.

Ismunadji

and Dijkshoorn

Nitrogen nutrition of rice plants measured by growth and nutrient content in pot experiments. 1. Ionic balance and selective uptake. Neth J Agric Sci 1971; 19(4): 223–236. DOI: 10.18174/njas.v19i4.17303.

35.

George

, Horst

and Neumann

Adaptation of plants to adverse chemical soil conditions. In: Marschner’s mineral nutrition of higher plants . Massachusetts: Academic Press, 2012, pp. 409–472.

36.

Zohlen

and Tyler

Soluble inorganic tissue phosphorus and calcicole–calcifuge behaviour of plants. Ann Bot 2004; 94(3): 427–432. DOI: 10.1093/aob/mch162, PMID 15277247.

37.

Manthey

, Crowley

and Luster

DG.

Biochemistry of metal micronutrients in the rhizosphere . Boca Raton: CRC Press, 1994.

38.

Ingrouille

Historical ecology of the British flora . London: Springer Science Business Media, 2012.

39.

Sterner

The continental element in the flora of south Sweden. Geogr Ann 1922; 4(3–4): 221–444. DOI: 10.1080/20014422.1922.11881061.

40.

Callow

JA.

Preface. Adv Bot Res 1999; 30: xxi–xxii. DOI: 10.1016/S0065-2296(08)60225-6.

41.

Gao

, Wang

, Ranathunge

, . Edaphic niche characterization of four Proteaceae reveals unique calcicole physiology linked to hyper-endemism of grevillea thelemanniana. New Phytol 2020; 228(3): 869–883. DOI: 10.1111/nph.16833, PMID 32726881.

42.

Lux

, Kohanová

and White

PJ.

The secrets of calcicole species revealed. J Exp Bot 2021; 72(4): 968–970. DOI: 10.1093/jxb/eraa555, PMID 33626153.

43.

Kim

, Kwak

and Mun

HT.

Classification of calcicoles and calcifuges on the basis of the ratio of soluble to insoluble Ca²⁺ and Mg²⁺ in the leaves. Korean J Ecol 1992; 15(3): 311–328.

44.

Gastón

, Soriano

and Gómez-Miguel

Lithologic data improve plant species distribution models based on coarse-grained occurrence data. Forest Syst 2009; 18(1): 42–49. DOI: 10.5424/fs/2009181-01049.

45.

Barth

JG.

Limestone and calcium in plants. Elem Naturwiss 2020; 112: 29–78.

46.

Duchaufour

Handbook of pedology . Cape Town: CRC Press, 2020.

47.

Singh

Biodiversity, conservation and systematics . Rajasthan, India: Scientific Publishing, 2019.

48.

Wei

, Deng

, Xiang

, . Calcium content and high calcium adaptation of plants in karst areas of southwestern Hunan, China. Biogeosciences 2018; 15(9): 2991–3002. DOI: 10.5194/bg-15-2991-2018.

49.

Rainbow

PS.

Heavy metals in barnacles. In: Barnacle biology . London: Routledge, 2018, pp. 405–417. DOI: 10.1201/9781315138053-21

50.

Jorgensen

and Fath

BD.

Encyclopedia of ecology . Newnes : Oxford.

51.

Ingestad

Mineral nutrient requirements of cucumber seedlings. Plant Physiol 1973; 52(4): 332–338. DOI: 10.1104/pp.52.4.332, PMID 16658558.

52.

Porley

RD.

England’s rare mosses and liverworts: their history, ecology, and conservation . USA: Princeton University Press, 2013.

53.

Botanical Society of Edinburgh. Transactions of the and proceedings of the botanical society of Edinburgh. The society, 1863.

54.

Zohlen

and Tyler

Immobilization of tissue iron on calcareous soil: differences between calcicole and calcifuge plants. Oikos 2000; 89(1): 95–106. DOI: 10.1034/j.1600-0706.2000.890110.x.

55.

Godwin

The history of the British Flora . UK: Cambridge University Press, 1956.

56.

Shimizu

Studies on the limestone flora of Japan and Taiwan . Kyoto: Kyoto University, 1963.

57.

Marquand

CV.

A bryological holiday in the Eastern Alps. Bryologist 1931; 34(2): 23–26.

58.

Smith

and Smith

TM.

Elements of ecology . CA: Benjamin-Cummings, Menlo Park, 1998.

59.

Xue

, Ren

, Long

, . Ecophysiological responses of calcicole Cyclobalanopsis glauca (Thunb.) oerst. to drought stress and calcium supply. Forests 2018; 9(11): 667. DOI: 10.3390/f9110667.

60.

Clymo

RS.

An experimental approach to part of the calcicole problem. J Ecol 1962; 50(3): 707–731. DOI: 10.2307/2257478.

61.

Paul

, Hauck

and Leuschner

Iron and phosphate uptake explains the calcifuge–calcicole behavior of the terricolous lichens Cladonia furcata subsp. furcata and C. rangiformis. Plant Soil 2009; 319(1–2): 49–56. DOI: 10.1007/s11104-008-9848-1.

62.

Cheek

, Luke

, Matimele

, . Cola species of the limestone forests of Africa, with a new, endangered species, Cola cheringoma (Sterculiaceae), from Cheringoma, Mozambique. Kew Bull 2019; 74(4): 1–4. DOI: 10.1007/s12225-019-9840-3.

63.

Fitter

and Hay

RK.

Environmental physiology of plants . Massachusetts: Academic Press, 2012.

64.

Lüttge

and Pitman

editors. Transport in plants II: Part B tissues and organs . Springer Science+Business Media, 2012.

65.

Liao

, Liang

, Jiang

, . Growth performance and element concentrations reveal the calcicole-calcifuge behavior of three Adiantum species. BMC Plant Biol 2020; 20(1): 327. DOI: 10.1186/s12870-020-02538-6, PMID 32650742.

66.

de Groot

, Korpelainen

, Wubs

, . Isolation of polymorphic microsatellite markers and tests of cross-amplification in four widespread European calcicole ferns. Am J Bot 2011; 98(11): e319–e322. DOI: 10.3732/ajb.1100051, PMID 22012927.

67.

Kruckeberg

AR.

Geology and plant life: the effects of landforms and rock types on plants . Seattle: University of Washington Press, 2004.

68.

Horovitz

Edaphic factors and flower colour distribution in the Anemoneae (Ranunculaceae). Plant Syst Evol 1976; 126(3): 239–242. DOI: 10.1007/BF00983363.

69.

Paun

, Schönswetter

, Winkler

, . Historical divergence vs. contemporary gene flow: evolutionary history of the calcicole Ranunculus alpestris group (Ranunculaceae) in the European Alps and the Carpathians. Mol Ecol 2008; 17(19): 4263–4275. DOI: 10.1111/j.1365-294x.2008.03908.x, PMID 19378404.

70.

Hemantaranjan

Environmental physiology . Rajasthan, India: Scientific Publishing, 2007.

71.

Dell’Orto

, De Nisi

, Pontiggia

, . Fe deficiency responses in Parietaria diffusa: a calcicole plant. J Plant Nutr 2003; 26(10–11): 2057–2068. DOI: 10.1081/PLN-120024264.

72.

Venturas

, Fernández

, Nadal

, . Root iron uptake efficiency of Ulmus laevis and U. minor and their distribution in soils of the Iberian Peninsula. Front Plant Sci 2014; 5: 104. DOI: 10.3389/fpls.2014.00104, PMID 24723927.

73.

Lousley

editor. The changing flora of Britain: being the report of the conference held in 1952 by the Botanical Society of the British Isles. Botanical Society of the British Isles.

74.

Kobiv

Saxifraga aizoides (Saxifragaceae) in Ukraine. Pol Bot J 2016; 61(1): 65–71. DOI: 10.1515/pbj-2016-0004.

75.

Kinzel

and Lechner

The specific mineral metabolism of selected plant species and its ecological implications. Bot Acta 1992; 105(5): 355–361. DOI: 10.1111/j.1438-8677.1992.tb00312.x.

76.

De Silva

and Mansfield

TA.

The stomatal physiology of calcicoles in relation to calcium delivered in the xylem sap. Proc R Soc Lond B 1994; 257(1348): 81–85. DOI: 10.1098/rspb.1994.0097.

77.

Blaschke

Multiple mycorrhizal associations of individual calcicole host plants in the alpine grass-heath zone. Mycorrhiza 1991; 1(1): 31–34. DOI: 10.1007/BF00205899.

78.

Lapeyrie

The role of ectomycorrhizal fungi in calcareous soil tolerance by “symbiocalcicole” woody plants. Ann Sci Forestières 1990; 47(6): 579–589. DOI: 10.1051/forest:19900604.

79.

Bolan

, Hedley

and White

RE.

Processes of soil acidification during nitrogen cycling with emphasis on legume-based pastures. Plant Soil 1991; 134(1): 53–63. DOI: 10.1007/BF00010717.

80.

Ström

, Owen

, Godbold

, . Organic acid behaviour in a calcareous soil implications for rhizosphere nutrient cycling. Soil Biol Biochem 2005; 37(11): 2046–2054. DOI: 10.1016/j.soilbio.2005.03.009.

81.

Dighton

Fungi in ecosystem processes . CRC Press, 2018.

82.

Prasad

, Shivay

and Kumar

Agronomic biofortification of cereal grains with iron and zinc. Adv Agron 2014; 125: 55–91. DOI: 10.1016/B978-0-12-800137-0.00002-9.

83.

Römheld

The role of phytosiderophores in acquisition of iron and other micronutrients in Graminaceous species: an ecological approach. In: Iron nutrition and interactions in plants. Proceedings of the fifth international symposium on iron nutrition and interactions in plants, Jun 11-17 1989, Jerusalem, Israel. Springer Netherlands; 1989 1991. pp. 159–66.

84.

Dotaniya

, Meena

, Lata

, . Role of phytosiderophores in iron uptake by plants. Agric Sci Dig A Res J 2013; 33(1): 73–76.

85.

Grillet

and Schmidt

The multiple facets of root iron reduction. J Exp Bot 2017; 68(18): 5021–5027. DOI: 10.1093/jxb/erx320, PMID 29036459.

86.

Gries

, Klatt

and Runge

Copper-deficiency-induced phytosiderophore release in the calcicole grass Hordelymus europaeus. New Phytol 1998; 140(1): 95–101. DOI: 10.1046/j.1469-8137.1998.00250.x.

87.

Gries

and Runge

Responses of calcicole and calcifuge Poaceae species to iron-limiting conditions. Bot Acta 1995; 108(6): 482–489. DOI: 10.1111/j.1438-8677.1995.tb00525.x.

88.

Lapeyrie

and Bruchet

Calcium accumulation by two strains, calcicole and calcifuge, of the mycorrhizal fungus Paxillus involutus. New Phytol 1986; 103(1): 133–141. DOI: 10.1111/j.1469-8137.1986.tb00602.x.

89.

Charisios

, Cotsopoulos

and Psaras

GK.

Distribution of calcium in epidermal cell types of Mediterranean xeromorphic calcicoles. Flora Morphol Distrib Funct Ecol Plants 2003; 198(5): 341–348. DOI: 10.1078/0367-2530-00106.

90.

Huang

, Liao

and Kirchoff

BK.

Calcium distribution and function in the glandular trichomes of Lavandula pinnata L. J Torrey Bot Soc 2010; 137(1): 1–15. DOI: 10.3159/09-RA-046.1.

91.

Gautam

, Tsai

and Schmidt

IRONMAN tunes responses to iron deficiency in concert with environmental pH. Plant Physiol 2021; 187(3): 1728–1745. DOI: 10.1093/plphys/kiab329, PMID 34618058.

92.

Grime

and Lloyd

PS.

An ecological atlas of grassland plants . UK: Hodder & Stoughton Educational, 1973.

93.

Ellenberg

Indicator values of vascular plants in central Europe . Scripta Geobotanica, Vol. 9, 1974.

94.

Ellenberg

, Weber

, Dull

, . Zeigerwerte von Pflanzen in Mitteleuropa . Göttingen: Goltze, 1992.

95.

Landolt

zur Schweizer Flora OZ, 1977.

96.

Chytrý

, Tichý

, Dřevojan

, . Ellenberg-type indicator values for the Czech flora. Preslia 2018; 90(2): 83–103. DOI: 10.23855/preslia.2018.083.

97.

Hill

, Roy

, Mountford

, . Extending Ellenberg’s indicator values to a new area: an algorithmic approach. J Appl Ecol 2000; 37(1): 3–15. DOI: 10.1046/j.1365-2664.2000.00466.x.

98.

Domina

, Galasso

, Bartolucci

, . Ellenberg indicator values for the vascular flora alien to Italy. Flora Mediterr 2018; 28(1): 53–61. DOI: 10.7320/FlMedit28.053.

99.

Tyler

, Herbertsson

, Olofsson

, . Ecological indicator and traits values for Swedish vascular plants. Ecol Indic 2021; 120: 106923. DOI: 10.1016/j.ecolind.2020.106923.

100.

Lawesson

, Fosaa

and Olsen

Calibration of Ellenberg indicator values for the Faroe Islands. Appl Veg Sci 2003; 6(1): 53–62. DOI: 10.1111/j.1654-109X.2003.tb00564.x.

101.

Dwyer

, Millett

, Pakeman

, . Environmental modifiers of the relationship between water table depth and Ellenberg’s indicator of soil moisture. Ecol Indic 2021; 132: 108320. DOI: 10.1016/j.ecolind.2021.108320.

102.

Ewald

The sensitivity of Ellenberg indicator values to the completeness of vegetation relevés. Basic Appl Ecol 2003; 4(6): 507–513. DOI: 10.1078/1439-1791-00155.

103.

Nuamah

Understanding Ellenberg indicator values; April 2024. Available from: https://owlcation.com/stem/Understanding-Ellenberg-Indicator-Values-For-Beginners.

104.

Leuenberger

Stable isotopes in tree rings as climate and stress indicators. vdf Hochschulverlag AG, 1998.

105.

Nakhutsrishvili

, Batsatsashvili

, Rudmann-Maurer

, . New indicator values for Central Caucasus flora. In: Plant diversity in the central great Caucasus: a quantitative assessment . Cham: Springer, 2017, pp. 145–160. DOI: 10.1007/978-3-319-55777-9_6.

106.

Wohlgemuth

and Gigon

Calcicole plant diversity in Switzerland may reflect a variety of habitat templets. Folia Geobot 2003; 38(4): 443–452. DOI: 10.1007/BF02803251.

107.

Nguyen

, Nguyen

, Chandran

, . Phytochemical, cardiovascular effect, antioxidant, antiinflammation and antitumor properties by Beta vulgaris (beet) root juice. J Transl Sci 2018; 5(5): 1–5. DOI: 10.15761/JTS.1000293.

108.

Zidorn

, Dirsch

, Rüngeler

, . Anti-inflammatory activities of hypocretenolides from Leontodon hispidus. Planta Med 1999; 65(8): 704–708. DOI: 10.1055/s-1999-14046, PMID 10630109.

109.

D′Angiolo

, De Leo

, Camangi

, . Chemical constituents of Ulmus minor subsp. minor fruits used in the Italian phytoalimurgic tradition and their anti-inflammatory activity evaluation. Planta Med 2022; 88(9–10): 762–773. DOI: 10.1055/a-1787-1342, PMID 35240714.

110.

Ouerfelli

, Majdoub

, Aroussi

, . Phytochemical screening and evaluation of the antioxidant and anti-bacterial activity of Woundwort (Anthyllis vulneraria L.). Rev Bras Bot 2021; 44(3): 549–559. DOI: 10.1007/s40415-021-00736-6.

111.

Dunkić

, Kosalec

, Kosir

, . Antioxidant and antimicrobial properties of Veronica spicata L. (Plantaginaceae). Curr Drug Targets 2015; 16(14): 1660–1670. DOI: 10.2174/1389450116666150531161820, PMID 26028041.

112.

Saha

, Kalia

, Sureja

, . Genetic analysis of bioactive compounds and antioxidant properties in lettuce (Lactuca sativa). Indian J Agri Sci 2016; 86(11): 1471–1476. DOI: 10.56093/ijas.v86i11.62931.

113.

Moshawih

, Abdullah Juperi

, Paneerselvam

, . General health benefits and pharmacological activities of Triticum aestivum L. Molecules 2022; 27(6): 1948. DOI: 10.3390/molecules27061948, PMID 35335312.

114.

Otang-Mbeng

and Sagbo

IJ.

Anti-melanogenesis, antioxidant and anti-tyrosinase activities of Scabiosa columbaria L. Processes 2020; 8(2): 236. DOI: 10.3390/pr8020236.

115.

Açıkgöz

, Karaltı

, Ersöz

, . Screening of antimicrobial activity and cytotoxic effects of two Cladonia species. Z Naturforsch C J Biosci 2013; 68(5–6): 191–197. DOI: 10.1515/znc-2013-5-604, PMID 23923615.

116.

Aljančić

, Vajs

, Menković

, . Flavones and sesquiterpene lactones from Achillea atrata subsp. multifida: antimicrobial activity. J Nat Prod 1999; 62(6): 909–911. DOI: 10.1021/np980536m, PMID 10395518.

117.

Lan

, Li

, Zhu

, . Flavonoids from Artemisia rupestris and their synergistic antibacterial effects on drug-resistant Staphylococcus aureus. Nat Prod Res 2021; 35(11): 1881–1886. DOI: 10.1080/14786419.2019.1639182, PMID 31303068.

118.

Bahadori

, Mahmoodi Kordi

, Ali Ahmadi

, . Antibacterial evaluation and preliminary phytochemical screening of selected ferns from Iran. Res J Pharmacogn 2015; 2(2): 53–59.

119.

Sharonova

, Nikitin

, Terenzhev

, . Comparative assessment of the phytochemical composition and biological activity of extracts of flowering plants of Centaurea cyanus L., Centaurea jacea L. and Centaurea scabiosa L. Plants 2021; 10(7): 1279.

120.

Sadowska

, Budzyńska

, Więckowska-Szakiel

, . New pharmacological properties of Medicago sativa and Saponaria officinalis saponin-rich fractions addressed to Candida albicans. J Med Microbiol 2014; 63(8): 1076–1086. DOI: 10.1099/jmm.0.075291-0, PMID 24850879.

121.

Martin

, Moran

and San Roman

Pharmacological screening of Pulsatilla alpina subsp. apiifolia. J Ethnopharmacol 1987; 21(2): 201–206. DOI: 10.1016/0378-8741(87)90132-2, PMID 3437772.

122.

Shah

, Patel

, . Antiurolithiatic and antioxidant activity of Hordeum vulgare seeds on ethylene glycol-induced urolithiasis in rats. Indian J Pharmacol 2012; 44(6): 672–677. DOI: 10.4103/0253-7613.103237, PMID 23248392.

123.

El Gamal

, AlSaid

, Raish

, . Beetroot (Beta vulgaris L.) extract ameliorates gentamicin-induced nephrotoxicity associated oxidative stress, inflammation, and apoptosis in rodent model. Mediators Inflamm 2014; 2014: 983952. DOI: 10.1155/2014/983952, PMID 25400335.

124.

Cuccioloni

, Bonfili

, Mozzicafreddo

, . Sanguisorba minor extract suppresses plasmin-mediated mechanisms of cancer cell migration. Biochim Biophys Acta 2012; 1820(7): 1027–1034. DOI: 10.1016/j.bbagen.2012.02.002, PMID 22348918.

125.

Corradi

, Schmidt

, Räber

, . Metabolite profile and antiproliferative effects in HaCaT cells of a Salix reticulata extract. Planta Med 2017; 83(14–15): 1149–1158. DOI: 10.1055/s-0043-109098, PMID 28449181.

126.

Panizo-Casado

, Déniz-Expósito

, Rodríguez-Galdón

, . The chemical composition of barley grain (Hordeum vulgare L.) landraces from the Canary Islands. J Food Sci 2020; 85(6): 1725–1734. DOI: 10.1111/1750-3841.15144, PMID 32484938.

Reclaiming Calcicoles: New Insights into Lime Lovers

Abstract

Keywords

Introduction

Calcicoles

Methodology

Calcicole v/s Calcifuge

Comparison Between Calcicole and Calcifuge.

Classification of Calcicoles

Classification of Calcicoles.

Distribution of Calcicoles

Distribution of Calcicoles.

Adaptive Mechanism of Calcicoles

Indexes and Indicator Values

Index of Calcifugy

Calcifuge Index (IC) Values of Different Plant Species Predicted by Cross and Lambers, 2021.

Ellenberg’s Indicator Values

Ellenberg Indicator Values.

Landolt Indicator Values

Phytopharmacological Status of Calcicoles

Anti-inflammatory Activity

Antioxidant Activity

Antimicrobial Activity

Other Pharmacological Activities

Reported Phytopharmacological Potential of Calcicoles.

Conclusion and Future Perspectives

Abbreviations

Footnotes

Acknowledgments

Declaration of Conflicting Interests

Ethical Statement

Funding

Informed Consent

ORCID iDs

References